Gamma-phase shifting in awake monkey visual cortex

Abstract

Gamma-band synchronization is abundant in nervous systems. Typically, the strength or precision of gamma-band synchronization is studied. However, the precise phase with which individual neurons are synchronized to the gamma-band rhythm might have interesting consequences for their impact on further processing and for spike timing-dependent plasticity. Therefore, we investigated whether the spike times of individual neurons shift systematically in the gamma cycle as a function of the neuronal activation strength. We found that stronger neuronal activation leads to spikes earlier in the gamma cycle, i.e., we observed gamma-phase shifting. Gamma-phase shifting occurred on very rapid timescales. It was particularly pronounced for periods in which gamma-band synchronization was relatively weak and for neurons that were only weakly coupled to the gamma rhythm. We suggest that gamma-phase shifting is brought about by an interplay between overall excitation and gamma-rhythmic synaptic input and has interesting consequences for neuronal coding, competition, and plasticity.

Figure 1.

Spike–LFP phase-locking spectra. A, Monkey J. Average spike–LFP phase-locking value plotted as function of frequency. Shaded regions indicate 95% confidence intervals around the mean. A gamma-band peak is visible at ∼67 Hz. B, Monkey L. Same conventions as in A. A gamma-band peak is visible at ∼40 Hz. C, Monkey N. Same conventions as in A. A gamma-band peak is visible at ∼40–53 Hz.

Figure 2.

Match between stimulus orientation and neuronal orientation preference determines spike phase in the gamma cycle. A, B, Data from one example neuron. A, Firing rate as a function of stimulus orientation. B, The black sine wave at the top and the sinusoidal gray shading in the background illustrate the LFP gamma phase. The colored lines show spike densities as a function of phase in the gamma cycle. The colors correspond to the colors used in the firing rate panel on the left. All spike density curves are probability densities, normalized such that the mean value of each curve is 1/2π (bottom left calibration bar applies to all curves, and curves are offset along the y-axis to correspond to A).

Figure 3.

Population results for orientation-dependent phase shift. Scatter plot of mean spike phase for the four least preferred orientations (x-axis) versus mean spike phase for the two most preferred orientations (y-axis). Every dot represents a single unit.

Figure 4.

Temporal evolution of spike density and spike phase during the trial. A–C, Data from one example neuron. A, Spike density as a function of time after stimulus onset, calculated in 250 ms rectangular windows. The fluctuations in spike density are predominantly driven by the onset transient and the position of the drifting grating over the receptive field of the neuron. B, Same analysis but for the spike phase in the gamma cycle. C, Same data as in A and B but now showing spike phase directly as a function of spike density.

Figure 5.

The relationship between spike density and spike phase. A, Example neuron. Spike phase in the gamma cycle plotted as a function of spike density. Colors represent normalized density. B, Group result. Distribution of linear–circular phase-shift regression parameter across neurons. Red bars indicate significant regression weights. Distribution is clearly skewed to the left. C–E, Comparison of frequencies. Average t statistic of spike phase onto spike density regression plotted as a function of frequency. For each monkey, gamma-phase shifting is most significant in that monkey's individual gamma-frequency band (compare with Fig. 1). Red squares indicate significant mean t statistic values (two-sided t test).

Figure 6.

Relationship between strength of rhythmic input and gamma-phase shifting. A, Group result. Mean spike phase in gamma cycle averaged across all neurons plotted as a function of spike density percentile. Filled region indicates 95% confidence intervals. B, Group result. Relationship between spike density percentile and spike phase in gamma cycle for trials with high power (red) versus trials with low power (blue). C, Mean spike phase in gamma cycle during fixation baseline period averaged across all neurons plotted as a function of spike density percentile. Filled region indicates 95% confidence intervals. D, Relationship between spike density percentile and spike phase in gamma cycle separate for neurons with strong phase locking (red) versus weak phase locking (blue).